Journal of Food Quality and Hazards Control 8 (2021) 13-20

Microbial Safety of Black Summer Truffle Collected from Sicily and Umbria Regions, Italy F. Cirlincione 1, N. Francesca 1* , L. Settanni 1, D. Donnini 2, G. Venturella 1, M.L. Gargano 3 1. Dipartimento Scienze Agrarie, Alimentari e Forestali, Università degli Studi di Palermo, Viale delle Scienze 4, 90128 Palermo , Italy 2. Dipartimento di Scienze Agrarie, Alimentari ed Ambientali, Università degli Studi di Perugia Borgo XX giugno, 74-06121 Perugia, Italy 3. Dipartimento di Scienze Agrarie e Ambientali, Università degli Studi di Bari “Aldo Moro”, Via Amendola 165/A, I-70126 Bari, Italy

HIGHLIGHTS  High microbial loads were detected in fresh ascomata of black summer truffles collected from Central Italy.  Pseudomonas spp. and lactic acid bacteria were present at the highest levels.  Common brushing procedure applied for preparation of truffles is not sufficient to eliminate microbial risks.

Article type ABSTRACT Original article Background: Tuber aestivum Vittad., known as black summer truffle, represents Keywords high-value food especially used as garnishment in nouvelle cuisine. The aim of this study Agaricales was to investigate on the viable microbial populations associated with T. aestivum Fungi Colony Count, Microbial ascomata collected in different sites of Sicily and one locality of Umbria (Italy). Food Microbiology Methods: The ripe ascomata of black summer truffles were collected from Central Italy. Food Safety Cell densities of spoilage bacteria, fecal indicators, potential pathogens, yeasts, and molds Italy were analyzed. Statistical analysis was conducted with XLSTAT software.

Article history Results: The microbiological counts of truffles ranged between 6.00 and 9.63 log Colony Received: 17 Jun 2020 Forming Unit (CFU)/g for total mesophilic count and between 6.18 and 8.55 log CFU/g Revised: 1 Oct 2020 for total psychrotrophic count; pseudomonads were in the range 6.98-9.28 log CFU/g. Accepted: 27 Oct 2020 Listeria spp. and coagulase-positive streptococci detected in no samples. Coagulase- negative streptococci were found in some samples with 2.11-4.76 log CFU/g levels. Acronyms and abbreviations CFU=Colony Forming Unit Yeasts and filamentous fungi were detected at consistent levels of 3.60-7.81 log CFU/g. CNS=Coagulase-Negative Significant differences (p<0.01) were found between samples and also for all microbial Staphylococci groups. CPS=Coagulase-Positive Staphy- lococci Conclusion: This study evidenced that the common brushing procedure applied for LAB=Lactic Acid Bacteria preparation of truffles is not sufficient to eliminate microbial risks for consumers. The TMC=Total Mesophilic Count application of an efficient decontamination treatment is strongly suggested before TPC=Total Psychrotrophic Count consumption of fresh truffles. © 2021, Shahid Sadoughi University of Medical Sciences. This is an open access article

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Introduction

Truffles are symbiotic fungi which grow in association vance in ecosystem because improves nutrition and with the roots of broad-leaved and conifer trees in health of plant (Buscot et al., 2000; Martin et al., 2001; ectomycorrhizal associations. This type of associations, Read, 1991). Truffles are essential for agronomy and prevalent in boreal and temperate forests, has high rele- forestry and the ascomata of some Tuber species, being

* Corresponding author (N. Francesca)  E-mail: [email protected] ORCID ID: https://orcid.org/0000-0002-6063-0130 To cite: Cirlincione F., Francesca N., Settanni L., Donnini D., Venturella G., Gargano M.L. (2021). Microbial safety of black summer truffle collected from Sicily and Umbria regions, Italy. Journal of Food Quality and Hazards Control. 8: 13-20.

DOI: 10.18502/jfqhc.8.1.5458 Journal website: http://www.jfqhc.com

Cirlincione et al.: Microbial Safety of Truffle Collected from Italy

edible, are more and more requested for their organolep- removing. An example of the truffle samples ready to tic properties (Zambonelli et al., 2014). be analyzed is reported in Figure 1. In order to avoid The most common truffle species collected in Italy is cross-contamination among samples, the brushing Tuber aestivum, known as black summer truffles or procedure was performed under a laminar flow hood and “scorzone” (Calvo et al., 2020; Comi et al., 2010, the brush was washed, rinsed with ethanol and subjected Venturella et al., 2011). Truffles ectomycorrhizas and to 30 min UV treatment before brushing the truffles of fruiting bodies harbor a different microbial community the different sites. including bacteria, yeasts, and filamentous fungi (Barbieri et al., 2005, 2007; Buzzini et al., 2005; Pacioni Microbiological analysis et al., 2007). Similarly to vegetables, the contamination Each sample (10 g) were aseptically collected and of truffles depends on several factors, especially wild transferred into sterile BagLight® 400 Multilayer® bags animals (including truffle dogs during ascomata collec- (Interscience, Saint Nom, France), made in PolySilk®. tion), air, and especially soil (Buck et al., 2003). Indeed, Ringer’s solution (Sigma-Aldrich, Milan, Italy) was add- soil hosts many bacterial populations, including human ed to reach a 10:1 dilution and the truffle samples were pathogen species that might be transferred to truffles homogenized by the stomacher BagMixer® 400 lab representing the most critical point for the safety of these blender (Interscience, Saint Nom, France) at the maxi- products. mum speed for 2 min. The aim of this study was to investigate on the viable Truffle samples were serially diluted (10:1 ratio) with microbial populations associated with T. aestivum Ringer’s solution (Sigma-Aldrich, Milan, Italy) and ascomata collected in different sites of Sicily and one investigated for the following 14 microbial groups locality of Umbria (Italy) which are generally sold in including Total Psychrotrophic Count (TPC), Total local markets without any decontamination procedure. Mesophilic Count (TMC); alterative microorganisms For this reason, the classical culture-dependent microbio- such as enterococci, pseudomonads, Coagulase-Negative logical approach was applied. Staphylococci (CNS), coccus and rods Lactic Acid Bacteria (LAB); pathogens such as Listeria spp. and enteric Gram-negative microorganism; alterative or Materials and methods potentially pathogens such as coliforms, members of the Enterobacteriaceae family, clostridia, Coagulase-Positive Samples Staphylococci (CPS); and eukaryotic microorganism The ripe ascomata of black summer truffles (T. such as yeasts and moulds. aestivum) were collected between June and November Cell suspensions were plated and incubated as follows: 2019 in different forest areas of Sicily (n=7) and a locali- TPC and TMC were spread plated on Plate Count Agar ty of Umbria (n=1) with the support of a trained dog. (PCA) and incubated aerobically at 22 °C for 7 days and Truffles were collected with their covering soil and 30 °C for 72 h, respectively; total coliforms were pour transported under refrigerated conditions by a thermal plated on Violet Red Bile Agar (VRBA), incubated insulated box containing reusable ice packs to the Labor- aerobically at 37 °C for 24 h; members of the atory of Agricultural Microbiology, Department of Agri- Enterobacteriaceae family were pour plated on Violet cultural, Food and Forestry Sciences (SAAF) of the Uni- Red Bile Glucose Agar (VRBGA), incubated aerobically versity of Palermo for analyses. Truffles weight ranged at 37 °C for 24 h; Pseudomonas species on Pseudomonas between 10 and 35 g, the shape was almost spherical with Agar Base (PAB) supplemented with Pseudomonas a diameter 4-6 cm, the external surface was dark and

Downloaded from jfqhc.ssu.ac.ir at 2:47 IRST on Friday September 24th 2021 [ DOI: 10.18502/jfqhc.8.1.5458 ] Cephaloridine-Fucidin-Cetrimide (CFC), incubated aero- covered by pyramidal warts; the internal pulp was com- bically at 20 °C for 48 h; enterococci on Kanamycin pact and aromatic. Truffle samples were named with the Aesculin Azide (KAA) agar, incubated aerobically at 37 code "TAR" followed by a progressive number according °C for 24 h; clostridia were first heated at 80 °C for 30 to reception order; specifically TAR 1, TAR 4, TAR 5, min in order to destroy the vegetative cells and then plat- TAR 7, and TAR 8 came from different site of Burgio ed on reinforced clostridial agar, incubated anaerobically (AG), TAR 2 from Castelbuono (PA), and TAR 9 from at 37 °C for 48 h; members of Listeria genus on Fraser Lucca Sicula (AG), all located in Sicily region, and TAR agar with specific supplement, incubated aerobically at 10 from Perugia (PG), the sole sample from Umbria re- 37 °C for 24 h; enteric Gram-negative on Hektoen gion. Before microbiological analyses, all samples were Enteric Agar (HEA), incubated aerobically at 37 °C brushed with a stainless steel mushroom brush (Ernesto, for 24 h; CPS and CNS on Baird Parker (BP) agar OWIM GmbH & Co. KG, Neckarsulm, Germany) with rabbit plasma fibrinogen supplement, incubated with soft plastic bristles to avoid damages during soil aerobically at 37 °C for 24 h; coccus LAB on M17 agar

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Journal of Food Quality and Hazards Control 8 (2021) 13-20

with cycloheximide (10 mg/ml) to avoid fungal growth, (Milan, Italy). Microbiological tests were carried out in incubated anaerobically at 30 °C for 48 h; rod LAB on de triplicate for each sample. Plate counts were determined Man-Rogosa-Sharpe (MRS) agar with cycloheximide, as Colony Forming Unit (CFU)/g and converted to

incubated anaerobically at 30 °C for 48 h; yeasts on log10 (log) values. The results were expressed as Yeast extract Peptone Dextrose (YPD) agar, incubated mean±Standard Deviation (SD). aerobically at 25 °C for 48 h and moulds on Malt Agar (MA), incubated aerobically at 25 °C for 7 days. To Statistical analyses inhibit bacterial growth, chloramphenicol (0.05 mg/ml) Statistical analyses were carried out with XLSTAT was added to YPD and MA; on the contrary, software version 7.5.2 for Excel (Addinsoft Inc., New cycloheximide (10 mg/ml) was added to MRS and M17 York, NY, USA). Means differences were calculated by to avoid fungal growth. Tukey's multiple-range test. Differences were considered All media and supplements were purchased from Oxoid significant at p<0.05.

Figure 1: A truffle sample after brushing

Downloaded from jfqhc.ssu.ac.ir at 2:47 IRST on Friday September 24th 2021 [ DOI: 10.18502/jfqhc.8.1.5458 ] Results The truffle samples of the different sites showed differ- ly, the sample TAR 9 showed TPC levels below the de- ent microbial loads for all investigated microbial groups. tection limit. Results of total and spoilage microorganism counts were Pseudomonads were in the range 6.98-9.28 log CFU/g shown in Table 1; and potentially pathogenic and eukar- and, also in this case, the sample TAR 9 resulted yotic microorganism counts were illustrated in Tables below the detection limit. Regarding LABs, cocci were 2 and 3, respectively. For all samples the highest cell found at higher levels than rods. Members of the densities were estimated on PCA incubated at 30 °C; Enterobacteriaceae family and, within this, total coli- TMC ranged between 6.00 and 9.63 log CFU/g. Howev- forms were detected in all samples at levels ranging from er, also TPC were particularly high for almost all samples 4.00 to 7.00 log CFU/g. Enterococci were present in all with loads between 6.18 and 8.55 log CFU/g. Surprising- truffles with values between 3.00 and 5.15 log CFU/g.

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Cirlincione et al.: Microbial Safety of Truffle Collected from Italy

Clostridia did not exceed 4.50 log CFU/g in the majority all samples, except TAR 7 and TAR 8; blue-green of samples, but were not detected in the samples TAR 2 colonies with black centre showing the potential presence and TAR 8. Listeria spp. was not detected in any of Salmonella spp. only in samples TAR 10 at 3.18 log samples. CPS neither were detected in any samples, but CFU/g. CNS were found in some samples (TAR 5, TAR 7, and Regarding the eukaryotic organisms, yeasts were de- TAR 9) with levels in the range 2.11 and 4.76 log CFU/g. tected at consistent levels (4.40-7.81 log CFU/g) in most Enteric Gram-negative count showed three different of the samples, but were not detected in samples TAR 1 morphologies on Hektoen Enteric Agar medium: red and TAR 4, while filamentous fungi were found in all colonies indicating the presence of presumptive Esche- samples except TAR 2 and TAR 10 at levels 3.60-4.65 richia coli in all samples; green colonies imputable to the log CFU/g. Significant differences (p<0.01) were found presence of presumptive Shigella spp. detected in almost between samples and also for all microbial groups.

Table 1: Total and spoilage microorganism counts of truffle samples

Table 2: Potentially pathogen microorganism loads of truffle samples Downloaded from jfqhc.ssu.ac.ir at 2:47 IRST on Friday September 24th 2021 [ DOI: 10.18502/jfqhc.8.1.5458 ]

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Table 3: Eukaryotic microorganism loads of truffle samples

Discussion The following work is the consequence of the hypothe- The presence of high levels of mesophilic microorgan- sis that truffles, because their development takes place isms can be imputable to the high temperatures registered inside soil and their consumption is mainly raw, can be during summer period in Italy, when T. aestivum harvest subject to high bacterial contamination, also in terms of occurs (Rivera et al., 2010). High temperatures are also potentially pathogenic bacteria for humans as reported in favorable to LAB development and this might explain the other previous work (Nazzaro et al., 2007; Rivera et al., high load of LAB cocci detected in all truffle samples 2011; Sorrentino et al., 2018). analyzed in our work. The cell densities of TPC were Results of microbiological analysis indicated TMC at lower than those recorded for TMC in all samples. No dominant levels up to 9.63 log CFU/g, followed by pseu- previous works on the microbiological characteristics of domonads and coccus LAB up to 9.28 log CFU/g. These truffles focused on the evaluation of the levels of TPC. results indicated that the main populations of truffles are However, TPC values detected in the present work coccus LAB and pseudomonads, typical spoilage bacteria followed the general trend observed for wild and of several foods of vegetable origin (Francesca et al., cultivated mushrooms. Gaglio et al. (2019) showed 2019; Miceli et al., 2019). Similar TMC levels were TPC loads in range of 6.85-7.86 log CFU/g in wild reported by other authors on truffle ascomata collected in mushrooms, comparable results were also showed by Molise region, Italy, and Aragon region, Spain (Comi et Jiang et al. (2018) who found mean load of 7.80 log al., 2010; Rivera et al., 2010; Sorrentino et al., 2013, CFU/g in sliced cultivated mushrooms. 2018). In particular, Comi et al. (2010) reported TMC The levels of pseudomonads estimated in the present

Downloaded from jfqhc.ssu.ac.ir at 2:47 IRST on Friday September 24th 2021 [ DOI: 10.18502/jfqhc.8.1.5458 ] loads of 9.50 log CFU/g in T. aestivum samples collected work are very similar to those recorded by Rivera et al. in Molise region, comparable to the loads found for TAR (2010) on whole T. aestivum (6.1-9.0 log CFU/g). Some 1, TAR 7, TAR 8, and TAR 10. Rivera et al. (2010) authors suggested that pseudomonads could have positive besides whole truffle, also investigated on the microbial action in the truffle life cycle (Bedini et al., 1999; Sbrana loads of gleba and peridium; as expected, the highest et al., 2002), but, after harvesting, they basically act mean loads (8.50 log CFU/g) of microorganisms were as spoilage microorganisms, especially for their revealed on the external part of truffles (peridum), almost psychrotrophic characteristics since they are able to mul- superimposable to the levels registered for samples TAR tiply at the low temperatures applied during storage. 2 and TAR 5. Other works analyzed microbiological Venturini et al. (2011) also showed that pseudomonads parameters of several mushrooms and shown similar could reach more than 90% of total counts in mushroom results of TMC in fresh wild or cultivated mushrooms samples. Furthermore, pseudomonads are more easily (Venturini et al., 2011) and in minimally processed sliced detected on mushroom species growing of compost (ex. mushrooms (Jiang et al., 2018; Kim et al., 2016). Agaricus bisporus) rather than on xylophagous species

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(ex. Lentinula edodes). Francesca et al. (2018) indicated general acceptability (Rivera et al., 2010, 2011). To this that Pseudomonas isolated from escarole and red chicory purpose, LAB strains characterised by antifungal proper- can be antibiotic resistant (especially to amoxicillin ties can be used to prevent the growth of molds on fresh and ampicillin). Sorrentino et al. (2018) suggested a truffles during the refrigerated storage (Sorrentino et al., treatment with gallic acid and refrigeration to reduce 2013). pseudomonads loads and inhibit the growth of other un- desirable microorganisms to elongate the shelf-life of truffles. Conclusion The natural truffle-grounds of Sicily do not limit the Although the microbiological characteristics of black access to domestic or wild animals, because they are summer truffles collected in woods and forests of various essential for the spread of truffle spores; thus, a fecal areas of Italy are known, this is the first survey aimed to contamination of the collected T. aestivum fruiting bodies characterize these products in Sicily. Specifically, this has to be considered. This risk is even amplified by the work evaluated the presence and cell densities of several higher presence of insects during the harvest period, microbial populations present on T. aestivum ascomata. promoting the proliferation of enteric bacteria also be- Due to the mode of collection (e.g. contact with trained cause the black summer truffle develops in the humic dogs) and post-harvest conditions applied during layer of soil, where microbial activity is particularly high transport and storage, the contamination of black summer (Rivera et al., 2010). For this reason, enterococci, total truffles does not exclusively depends on environmental coliforms, and members of Enterobacteriaceae family factors. have been object of the present investigation. The total The results of this work showed that total mesophilic coliform levels registered in the present work are almost populations were present at dominated levels and, in closed to those reported by Comi et al. (2010) for addition to alterative microorganisms (Pseudomonas spp. truffles collected in Molise region. The levels of and LAB); potentially pathogenic microorganisms such Enterobacteriaceae showed in our work are higher than as coliforms and members of Enterobacteriaceae (pre- those found on truffles by other authors (Nazzaro et al., sumptive E. coli, Shigella spp., and Salmonella spp.) 2007; Reale et al., 2009; Rivera et al., 2011). Similar were detected. Therefore, a deepen identification of the Enterobacteriaceae levels were also reported for wild and dominant bacteria is necessary to determine their allot- cultivated mushrooms (Venturini et al., 2011). This ting into pathogenic species, in order to confirm that group of microorganisms determines a decay of the or- black summer truffles might represent a risk for human ganoleptic and visual qualities of vegetables and includes health, also considering the low amount used for food species potentially pathogenic for humans (Alfonzo et al., garnishing. However, based on the high levels of viable 2018). microorganisms detected, a decontamination treatment in Our data showed cell densities of enterococci ranging addition to the common brushing is strongly suggested between 3.00 and 5.15 log CFU/g, higher than the values before truffle consumption. showed by Comi et al. (2010). Clostridia, when present, were in the same order of magnitude of those reported by Author contributions Comi et al. (2010) and Reale et al. (2009). Their presence may be associated with diseases, also serious, because N.F., L.S., and G.V. designed the project of study; F.C. they are able to synthesize toxins with different actions conducted the experimental work; M.L.G. and D.D. on the human health (Uzal et al., 2018). Listeria and CPS did the statistical analyses; F.C. and L.S. wrote the manu- were not detected in any sample, while E. coli and script. All authors read and approved the revised manu- Downloaded from jfqhc.ssu.ac.ir at 2:47 IRST on Friday September 24th 2021 [ DOI: 10.18502/jfqhc.8.1.5458 ] Shigella spp. were found in a few samples. Salmonella script. spp. was not found in Sicilian samples, and only detected in truffles collected in Umbria region. All these strains Conflicts of interest represent a risk for the fresh consumption of truffles. Regarding truffle associated eukaryotic microorganism, All the authors declared that there was no conflict of yeasts were found at variable levels in the different sam- interest in this study. ples, but always higher than those found by Comi et al. (2010) and Rivera et al. (2011). On the contrary, mold Acknowledgements levels, although variable among samples, were slightly lower than those reported by the previous works. Yeasts This research did not receive any specific grant from and molds during the storage of truffles might generate funding agencies in the public, commercial, or not-for off-flavours and affect their visual quality, taste, and profit sectors.

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